Killer Knots: Molecular Evolution of Inhibitor Cystine Knot Toxins in Wandering Spiders (Araneae: Ctenidae)
Abstract
:1. Introduction
2. Results
2.1. Venom Gland Transcriptome and Proteome
2.2. Phylogenetic Results
2.3. Inhibitor Cystine Knot Annotation
2.4. Disulfide Connectivity Predictions
2.5. Phylogenetic Tests for Selection
3. Discussion
4. Conclusions
5. Materials and Methods
5.1. Taxon Sampling
5.2. Venom and RNA Isolation
5.3. Sequencing and Processing
5.4. Transcript Reconstruction and Expression Quantification
5.5. Venom Proteomics
5.6. Locus Sampling
5.7. Phylogenetic Reconstruction
5.8. Inhibitor Cystine Knot Annotation
5.9. Disulfide Connectivity Predictions
- 1.
- DISULFIND collectively decides the bonding state assignment of the entire chain using a Support Vector Machine binary classifier followed by a refinement stage [25]. DISULFIND v1.1 was used to generate a total of three alternative disulfide connection predictions.
- 2.
- CYSCON uses a hierarchical order reduction protocol to identify the most confident disulfide bonds and then evaluate what remains using Support Vector Regression [26]. CYSCON v2015.09.27 was used to generate a single disulfide prediction per ICK representative per unique cysteine framework.
- 3.
- CRISP v1.0 not only predicts disulfide bonds, but also the entire structure of a cysteine rich peptide by searching a customized template database with cysteine-specific sequence alignment with three separate machine learning models to filter templates, rank models, and estimate model quality [27]. CRISP was used to generate five structural models for each ICK representative per unique cysteine framework.
5.10. Phylogenetic Tests for Selection
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Species | Sex | Sample | Transcripts | SuperTranscripts | CDS |
---|---|---|---|---|---|
Anahita punctulata | male | 297 | 120,048 | 88,950 | 55,238 |
Ctenus captiosus | female | 305 | 124,919 | 99,712 | 59,434 |
Ctenus captiosus | female | 311 | 140,647 | 110,550 | 64,437 |
Ctenus captiosus | male | 303 | 157,109 | 123,061 | 70,951 |
Ctenus captiosus | male | 306 | 158,795 | 122,878 | 71,795 |
Ctenus exlineae | female | 244 | 105,140 | 85,561 | 49,630 |
Ctenus exlineae | female | 245 | 111,981 | 89,516 | 52,365 |
Ctenus exlineae | female | 247 | 112,224 | 90,112 | 52,434 |
Ctenus exlineae | male | 242 | 95,088 | 78,974 | 44,942 |
Ctenus exlineae | male | 246 | 54,776 | 46,375 | 24,166 |
Ctenus hibernalis | female | 91 | 194,576 | 148,947 | 83,512 |
Ctenus hibernalis | female | 92 | 161,519 | 124,108 | 71,340 |
Ctenus hibernalis | male | 148 | 202,764 | 157,422 | 81,381 |
Leptoctenus byrrhus | female | 136 | 99,257 | 81,488 | 47,189 |
Leptoctenus byrrhus | male | 213 | 108,687 | 88,723 | 50,313 |
Leptoctenus byrrhus | male | 222 | 101,706 | 83,634 | 47,527 |
Species | Sex | Sample | Peptides | ICKs | %ICK | Sum TPM | ICK TPM | %TPM |
---|---|---|---|---|---|---|---|---|
C. exlineae | male | 242 | 113 | 5 | 4.42% | 18,214.3 | 9670.5 | 53.1% |
C. exlineae | female | 245 | 127 | 7 | 5.51% | 16,755.8 | 7002.0 | 41.8% |
C. exlineae | male | 246 | 200 | 13 | 6.50% | 131,454 | 51,011.1 | 38.8% |
C. exlineae | female | 244 | 339 | 5 | 1.47% | 42,546.4 | 12,227.6 | 28.7% |
C. exlineae | female | 247 | 194 | 5 | 2.58% | 27,378.7 | 5436.3 | 19.9% |
C. hibernalis | female | 4926 | 196 | 8 | 4.08% | 109,103 | 57,283.2 | 52.5% |
C. hibernalis | female | 91 | 525 | 12 | 2.29% | 111,759 | 14,703.9 | 13.2% |
C. hibernalis | male | 148 | 170 | 7 | 4.12% | 31,121.2 | 2581.5 | 8.3% |
C. hibernalis | female | 92 | 176 | 5 | 2.84% | 37,128.6 | 2366.6 | 6.4% |
Identifier | Dinez Numeral | Motif | Total |
---|---|---|---|
6.0 | I | ---- | 123 |
8.0 | II | ---- | 538 |
10.0 | V | ----- | 117 |
10.1 | ----- | 23 | |
12.0 | VI | ------- | 100 |
12.1 | VII | ------ | 27 |
14.0 | VIII | --------- | 33 |
Family | Species | 6.0 | 8.0 | 10.0 | 10.1 | 12.0 | 12.1 | 14.0 |
---|---|---|---|---|---|---|---|---|
Homalonychidae | Homalonychus theologus | 1 | 4 | 2 | 0 | 9 | 0 | 0 |
Salticidae | Habronattus signatus | 6 | 13 | 2 | 1 | 1 | 0 | 0 |
Xenoctenidae | Odo patricius | 2 | 21 | 2 | 0 | 3 | 0 | 0 |
Anyphaenidae | Hibana sp. | 3 | 10 | 0 | 1 | 1 | 0 | 0 |
Gnaphosidae | Sergiolus capulatus | 1 | 11 | 0 | 1 | 2 | 0 | 0 |
Thomisidae | Thomisus spectabilis | 2 | 13 | 3 | 0 | 2 | 0 | 1 |
Thomisidae | Misumenoides formosipes | 1 | 4 | 0 | 1 | 0 | 0 | 0 |
Oxyopidae | Oxyopes sp. | 0 | 15 | 9 | 0 | 2 | 0 | 0 |
Oxyopidae | Peucetia longipalpis | 1 | 11 | 4 | 1 | 0 | 0 | 0 |
Lycosidae | Hippasa holmerae | 1 | 11 | 5 | 1 | 3 | 0 | 0 |
Lycosidae | Pardosa pseudoannulata | 0 | 7 | 1 | 1 | 0 | 0 | 0 |
Lycosidae | Schizocosa rovneri | 0 | 10 | 0 | 0 | 1 | 0 | 0 |
Lycosidae | Sosippus placidus | 5 | 26 | 1 | 1 | 3 | 0 | 2 |
Pisauridae | Nilus albocinctus | 1 | 8 | 2 | 1 | 3 | 0 | 0 |
Pisauridae | Sphedanus quadrimaculatus | 1 | 6 | 2 | 1 | 4 | 0 | 0 |
Pisauridae | Pisaurina mira | 0 | 1 | 0 | 1 | 1 | 0 | 0 |
Pisauridae | Dolomedes triton | 1 | 11 | 0 | 0 | 10 | 0 | 1 |
Psechridae | Fecenia protensa | 1 | 17 | 4 | 0 | 2 | 1 | 1 |
Psechridae | Psechrus singaporensis | 0 | 13 | 3 | 1 | 2 | 1 | 0 |
Ctenidae | Ctenus corniger | 11 | 19 | 5 | 1 | 3 | 1 | 1 |
Ctenidae | Anahita punctulata | 2 | 15 | 1 | 0 | 2 | 1 | 1 |
Ctenidae | Ctenus captiosus | 4 | 10 | 2 | 1 | 3 | 1 | 2 |
Ctenidae | Ctenus exlineae | 2 | 9 | 2 | 1 | 2 | 1 | 1 |
Ctenidae | Ctenus hibernalis | 2 | 10 | 3 | 1 | 3 | 1 | 1 |
Ctenidae | Isoctenus sp. | 3 | 11 | 4 | 0 | 0 | 1 | 2 |
Ctenidae | Leptoctenus byrrhus | 1 | 12 | 2 | 1 | 1 | 1 | 1 |
Ctenidae | Phoneutria nigriventer | 5 | 12 | 3 | 0 | 1 | 1 | 2 |
Class | Loop 1 | Loop 2 | Loop 3 | Loop 4 |
---|---|---|---|---|
C6.0 | - | - | - | - |
C8.0 | - | - | - | - |
C10.0 | - | - | - | - |
C10.1 | - | - | -- | - |
C12.0 | - | - | - | - |
C12.1 | - | - | - | - |
C14.0 | - | - | - | - |
Model | log(likelihood) | Parameters | AICc | |||
---|---|---|---|---|---|---|
Unconstrained | −37,648.7 | 1169 | 77,691.4 | 0.06 | 0.09 | 3.35 |
Constrained | −37,733.9 | 1168 | 77,859.6 | 0.03 | 0.03 | 1.00 |
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Brewer, M.S.; Cole, T.J. Killer Knots: Molecular Evolution of Inhibitor Cystine Knot Toxins in Wandering Spiders (Araneae: Ctenidae). Toxins 2023, 15, 112. https://doi.org/10.3390/toxins15020112
Brewer MS, Cole TJ. Killer Knots: Molecular Evolution of Inhibitor Cystine Knot Toxins in Wandering Spiders (Araneae: Ctenidae). Toxins. 2023; 15(2):112. https://doi.org/10.3390/toxins15020112
Chicago/Turabian StyleBrewer, Michael S., and T. Jeffrey Cole. 2023. "Killer Knots: Molecular Evolution of Inhibitor Cystine Knot Toxins in Wandering Spiders (Araneae: Ctenidae)" Toxins 15, no. 2: 112. https://doi.org/10.3390/toxins15020112